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Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis
Open accessAbstract
Roland Brosch and colleagues report whole-genome sequencing of tubercle bacilli with smooth colony morphology, also known as Mycobacterium canetti and/or Mycobacterium prototuberculosis, obtained from humans with tuberculosis from geographically diverse regions. Their comparative genomic analysis with Mycobacterium tuberculosis and other M. tuberculosis complex members identifies extensive recombination and provides insights into the evolution of mycobacteria. The authors also report that tubercle bacilli with smooth colony morphology show reduced persistence and virulence compared to M. tuberculosis strains in infection experiments in mice. Global spread and limited genetic variation are hallmarks of M. tuberculosis, the agent of human tuberculosis. In contrast, Mycobacterium canettii and related tubercle bacilli that also cause human tuberculosis and exhibit unusual smooth colony morphology are restricted to East Africa. Here, we sequenced and analyzed the whole genomes of five representative strains of smooth tubercle bacilli (STB) using Sanger (4–5× coverage), 454/Roche (13–18× coverage) and/or Illumina DNA sequencing (45–105× coverage). We show that STB isolates are highly recombinogenic and evolutionarily early branching, with larger genome sizes, higher rates of genetic variation, fewer molecular scars and distinct CRISPR-Cas systems relative to M. tuberculosis. Despite the differences, all tuberculosis-causing mycobacteria share a highly conserved core genome. Mouse infection experiments showed that STB strains are less persistent and virulent than M. tuberculosis. We conclude that M. tuberculosis emerged from an ancestral STB-like pool of mycobacteria by gain of persistence and virulence mechanisms, and we provide insights into the molecular events involved.
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“That concept was challenged when the comparative analysis of multiple genome sequences of Mycobacterium canettii (a smooth colony outlier of the MTBC) revealed thousands of SNPs: the striking similarity to the experimentally produced mosaic genomes of M. smegmatis provided the first indication that HGT had occurred in the MTBC (48–51).”
From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [49]
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“representing a group of rare tubercle bacilli that are thought to resemble the ancestor of M. tuberculosis and have been isolated mainly from tuberculosis patients in the region of the Horn of Africa (East Africa) (56,57).”
From ESX/Type VII Secretion Systems—An Important Way Out for Mycobacterial Proteins (2019) · cites this paper as [56]
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ESX secretion systems: mycobacterial evolution to counter host immunity
Gröschel, M. I., Sayes, F., Simeone, R., Majlessi, L., & Brosch, R. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.131 · Cited by 382
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Metadata
- Authors
- Supply, P., Marceau, M., Mangenot, S., Roche, D., Rouanet, C., Khanna, V., Majlessi, L., Criscuolo, A., Tap, J., Pawlik, A., Fiette, L., Orgeur, M., Fabre, M., Parmentier, C., Frigui, W., Simeone, R., Boritsch, E. C., Debrie, A.-S., Willery, E., Walker, D., Quail, M. A., Ma, L., Bouchier, C., Salvignol, G., Sayes, F., Cascioferro, A., Seemann, T., Barbe, V., Locht, C., Gutierrez, M.-C., Leclerc, C., Bentley, S. D., Stinear, T. P., Brisse, S., Médigue, C., Parkhill, J., Cruveiller, S., & Brosch, R.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Institut Pasteur (FR)
- Inserm (FR)
- Hôpital d'instruction des Armées Percy (FR)
- Wellcome Sanger Institute (GB)
- Monash University (AU)
- The University of Melbourne (AU)
- Corresponding author
- Supply, Philip
- Brosch, Roland
- ORCID
- Supply, Philip
- Mangenot, Sophie
- Roche, David
- Rouanet, Carine
- Khanna, Varun
- Majlessi, Laleh
- Criscuolo, Alexis
- Tap, Julien
- Pawlik, Alexandre
- Frigui, Wafa
- Debrie, Anne-Sophie
- Quail, Michael A
- Ma, Laurence
- Bouchier, Christiane
- Salvignol, Grégory
- Sayes, Fadel
- Cascioferro, Alessandro
- Seemann, Torsten
- Barbe, Valérie
- Locht, Camille
- Gutierrez, Maria-Cristina
- Leclerc, Claude
- Bentley, Stephen D
- Stinear, Timothy P
- Brisse, Sylvain
- Médigue, Claudine
- Parkhill, Julian
- Cruveiller, Stéphane
- Brosch, Roland
- Venue
- Nature Genetics
- Published
- 2013-01-06
- Volume
- 45
- Issue
- 2
- Pages
- 172-179
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC3856870
- OpenAlex
- W2005360702
- Cited by
- 305
- References
- 66
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 11 · 2023: 18 · 2022: 12 · 2021: 24 · 2020: 25 · 2019: 21 · 2018: 12 · 2017: 27 · 2016: 30 · 2015: 39 · 2014: 44 · 2013: 15
- FWCI
- 31.13
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- www.springer.com/tdm (unspecified)
- Locations
- Nature Genetics (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Minerva Access (University of Melbourne) (submittedVersion)
- LillOA (Université de Lille (University Of Lille)) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (098051)
- European Commission (260872)
- Agence Nationale de la Recherche (ANR-10-INBS-0009)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Health Sciences › Medicine › Infectious Diseases › Infectious Diseases and Tuberculosis
- Keywords
- Mycobacterium tuberculosis, Mycobacterium tuberculosis complex, recombination, bacterial evolution, pathoadaptation, virulence, persistence, CRISPR-Cas, core genome, East Africa
- MeSH terms
- Adaptation, Biological, Animals, Base Sequence, Lung, Mice, Inbred BALB C, Molecular Sequence Data, Mycobacterium tuberculosis, Phylogeny, Species Specificity, Spleen, Genetic Variation, Virulence, Cluster Analysis, Genome, Bacterial, Sequence Analysis, DNA, Evolution, Molecular, Polymorphism, Single Nucleotide, Genomics, Mice, Inverted Repeat Sequences
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